As Charles Darwin sailed on his epic voyage, he noticed something which initially troubled him. In many species, the males had traits which seemed disadvantageous. In birds, for example, the females tended to be dull and camouflaged, whereas the males were often bright and garish. He was particularly impressed with extreme examples, such as the peacock. How, he wondered, is it possible that nature would select for peacocks to have such clearly disadvantageous traits like absurd colors and impossibly long tails? Fortunately, Darwin was a smart man, and he soon uncovered the answer: an evolutionary mechanism known as sexual selection.

I honestly found this post very hard to write, because I find sexual selection to be utterly fascinating and mesmerizing. There are so many cool facets to it and so many amazing examples that I wanted to share with you that writing a single, condensed post seemed nearly impossible. As a result, I have been forced to leave out a ton of great examples, and this post won’t be much more than a Cliff Notes introduction. I would encourage you, however, to study it more on your own. Also, if you want to see a bunch of neat examples, I cannot recommend David Attenborough’s documentaries strongly enough. They are fantastic.

What is sexual selection?Sexual selection is really best understood as a type of natural selection because it operates off of the same three requirements:
1). The trait is heritable
2). The trait is variable
3). The variation affects individuals’ ability to pass genetic material on to the next generation

Sexual selection also has an additional requirement, however. It deals specifically with the traits that are directly involved with obtaining a mate and forming a zygote (egg+sperm). Exactly what traits fall under the realm of sexual selection is somewhat of a grey area, but it is generally applied predominantly to sexual dimorphisms (i.e., anatomical differences between males and females), especially secondary sexual dimorphisms (i.e., dimorphisms that are involved in obtaining a mate, but not in the actual act of mating). This covers traits such as ornaments and colors that help many males to attract females, as well as features that help in conflict within the sexes (e.g. sexual selection is generally given credit for driving the evolution of antlers in the males of many deer species, because the antlers are used by the males to fight over females).

Sexual selection also differs from classical natural selection in one other important way. In classical natural selection, there isn’t actually an agent doing the selecting. Rather, it is simply a numbers game where the individuals who pass on the most genes are “selected” by simple virtue of the fact that they passed more genetic material into the next generation than their rivals did. Remember, evolution is simply a change in the allele frequencies of a population over time. So, getting a disproportionate number of your alleles into the next generation causes the allele frequencies to shift in your favour. In sexual selection, however, there often is an agent who is actually selecting traits. In many species, one sex (usually females) directly chooses who to mate with, which means that females are actually selecting which traits will become predominant in the population. This is fascinating because, as I will explain, it gives females the opportunity to guide selection, and it often results in them being real jerks (if you’ll forgive me for anthropomorphising).

Note: for most of this post, I am going to act as if females are the ones doing the selecting, but there are a few exceptions which I will discuss at the end.

Females often select for seemingly arbitrary traitsSometimes, the traits that females select make good sense. For example, females of many insect species demand a “nuptial gift” from their suitors. This is generally something edible, such as another insect, salt crystal, or even sperm (there is some debate about how beneficial these actually are for females; see Gwynne. 2008 for a review). For example, if you have ever seen a group of butterflies congregating around a drying mud puddle, many of those are actually males who are collecting salt crystals to present to potential mates.

Similarly, some birds select for sensible traits like nest construction. In other words, females are choosing their mates based on who makes the best nest. This makes good sense since a well- constructed nest increases the chance of her offspring surviving. In many other species, it is a male’s ability to defend a territory that interests females, and the females choose to mate with males who have large territories with adequate resources for rearing her young.

This bower belongs to a great bowerbird (Chlamydera nuchalis) that lives on my university’s campus. You’ll notice that in addition to constructing the bower itself (the columns of sticks) he has amassed a large collection of green, white, and grey objects. Some of his treasures are natural like rocks, dead coral, and shells, but he also has a lot of human trash like old nails, broken glass, and plastic.

For many species, however, the traits that females select initially appear arbitrary. Take color and call, for example. Why do females of so many species prefer their males to be brightly colored, and why do they care if the males make loud, long, complex calls? Other species go far beyond simply wanting calls and colors and demand complex dance routines or even decorations. The bowerbirds are one of my favorite examples of this (Attenborough has some great documentaries on these guys and you can see a clip from one here). In these species, the males build elaborate and often enormous structures called bowers, and they decorate them with all manner of trinkets. Exactly what gets used depends on both the species and the individual. Some species/individuals have a fascination with particular colors and may collect predominantly one color. Others are more eclectic and gather a diversity of objects. Regardless of the specifics, however, they all tend to be a bit OCD, and the males devote themselves to meticulously maintaining their collection. The females then fly around to different bowers and assess the males’ collections as well as their construction abilities, and they use those factors to decide who to mate with. Importantly, after mating, females do not stay at the bower. Rather, they fly off to make a nest and rear the young, while the males waits for more females. In other words, the bower is not a nest or a foraging area, and the females get nothing out of it except sperm. So, once again, why? Why do females care how large the males’ collection is?

Partial answers for these questions do, of course, exist, and, as I will explain, the selection for traits is not as arbitrary as it may initially seem.

The handicap principle and runaway selectionBefore I explain why females choose the traits that they do, I need to introduce two other pieces of the puzzle. First, let’s talk about the handicap principle. In short, this states that females generally choose traits that screw the males over. In other words, they are selecting traits that are disadvantageous for males. Think, once again, about colors and calls in birds. It is clearly not in the males’ best interest (as far as survivorship) to be brightly colored or to loudly announce your position to predators, yet the females want the loud, brightly colored males. Similarly, in species like bowerbirds, the males invest an incredible amount of energy and resources into building and maintaining a bower, and they could be spending that time and energy finding food.

The second principle is runaway selection. This states that there is essentially no limit to the females’ obsessive desire for improved traits. In other words, if a bright male is good, a brighter male is even better. The classic experiment on this was conducted on long-tailed widowbirds (Euplectes progne; Andersson 1982). Male widowbirds live in the African savannas and display for females by jumping and flying above the tall grass to display their absurdly long tails. Scientists suspected that tail length was important in mate choice. So, Andersson selected a group of males with similar tails and similar mating success. Then, he cut the tail feathers off of several males and glued them on to the tails of some of the other males. Thus, he had shortened tails, normal tails, and tails that were roughly twice their normal length. What he found, was that females weren’t thrilled about the short tails, would still mate with the normal tails, and were really turned on by the long tails (i.e., the birds with the extra-long tails got most of the mates).

Here, we have a situation with both the handicap principle and runaway selection. Having long tails is not good for the males because it makes it harder for them to fly, and it makes it easier for predators to pick them off. Nevertheless, despite (or perhaps because of) the disadvantages to the males, there doesn’t seem to be a limit on the females’ desire for long tails (the longer the better).

Why do females choose traits that are bad for males?At this point, we finally have enough pieces of the puzzle to start to put it together. There are several different hypotheses about why females choose the way that they do, but I will just discuss the two predominant ones. First up, we have the “sexy sons hypothesis” (yes, that is its actual name). This basically states that females select for traits that will maximize the reproductive potential of their offspring. In other words, if a female mates with a very attractive male, then her offspring will also be very attractive, which will allow them to get lots of mates (remember, if you don’t continue to get genes into the next generation, then you are evolutionarily dead).

At a quick glance, the sexy sons hypothesis makes good sense, but I am personally not a big fan because I don’t think that it actually answers anything. Consider the following.

1). A female is attracted to red
2). Therefore, she mates with a red male so that her offspring will also be red
3). Other females are also attracted to red
4). Therefore, her offspring will enjoy lots of mates

Do you see the problem? Why were females attracted to red in the first place? The sexy sons hypothesis basically says, “females are attracted to X because other females are attracted to X.” It’s circular, and I don’t like circular logic. To be clear, I’m not saying that the sexy sons hypothesis is worthless. I think that it may help to explain runaway selection, but I don’t think that it is an adequate ultimate explanation for why females choose the traits that they do.

A more compelling explanation (in my opinion) can be found in the “good genes hypothesis.” This proposes that females are using traits like colors and calls to judge whether or not the males have good genes. For example, a male that is able to produce brightly colored feathers and call loudly while still being able to avoid predators and forage successfully probably has good genes, which means that offspring from that male will also have good genes. This may sound superficially like the sexy sons hypothesis, but there is an important difference. In the sexy sons hypothesis, females are selecting a trait that they are attracted to because their sons will also get that attractive trait; whereas, in the good genes hypothesis, the females are simply using that trait as a way to assess whether or not a given male will produce high quality offspring.

The good genes hypothesis provides satisfying explanations for both the handicap principle and runaway selection. It proposes that females choose traits that are disadvantageous for males because that is the best way to actually judge the male. In other words, if females selected a trait that didn’t affect males one way or the other, that wouldn’t let them judge the quality of the males’ genes. In contrast, selecting a trait that is harmful for the males lets them judge the males, because only a male with good genes would be able to have the harmful trait and still survive. Further, it makes sense that a very exaggerated trait will be a better judge of a male’s quality than a minor trait. Thus, judging males on exaggerated traits could drive runaway selection (think back to the long-tailed widowbird experiment: the longer your tail, the harder it is to survive/avoid predators, but the more the females like you). All of this is, of course, predicated on the notion of “honest signalling.” In other words, this only works if the traits that females are selecting do actually reflect the males’ quality.

At this point, you may notice that there is still a problem. I have offered an explanation for why females choose disadvantageous traits, but I have not explained why they choose the particular disadvantageous traits that they do (e.g., why do female Northern Cardinals like red instead of a different color, like blue?). In short, we don’t really know, and there are probably lots of different factors that affect different species. In some cases, it may even be simply a random result of genetic drift, but other possibilities exist.

One really interesting possibility is what’s called a pre-existing sensory bias. For example, let’s say that a certain species eats mostly red berries. This could give them a pre-existing sensory bias for the color red (i.e. they like the color red). Then, after many generations of eating red berries, a male hatches with a mutation that causes him to have red feathers. Because of the pre-existing bias, the females will find that mutation very attractive, and he will get lots of mates. As a result, the mutation will become more common in the next generation and his offspring will benefit greatly from it. Thus, in each generation the mutation becomes more and more common, until eventually all of the males are red.

Sexual conflictIt should by now be clear that there is a conflict between sexual selection and natural selection which ultimately results in a battle of the sexes. On the one hand, female choice and sexual selection are driving males towards increasingly elaborate and disadvantageous traits. Meanwhile, classical natural selection is driving males away from those elaborate traits because they result in dead males. This results in a balance or equilibrium state between the two forces.

Let’s use a bird with a long tail as an example, and let’s say that the normal equilibrium tail length is 10cm, and individuals with 10cm tails have 5 offspring on average. Females would choose longer tails if they were available, but individuals with longer tails have such high predation rates that they don’t live long enough to mate often. As a result, individuals with tails >10cm actually only have four or fewer offspring before dying. Conversely, males will live longer if they have tails that are <10cm, but they won’t get as many mates. So, once again, they will have four or fewer offspring. This is an equilibrium state because longer tails get selected against because of low survivorship, and shorter tails get selected against because of low interest from the females.

There are many different factors that influence the equilibrium point, and it can change with the environment. For example, if a new predator gets introduced, that may cause the point to shift towards slightly shorter tails because survivorship becomes more important than female choice. Nevertheless, it is obvious that in many cases, the equilibrium point was reached in favor of the females, because as far as male survivorship is concerned, it would be best for the males to be just as plain and boring as the females. The reason that the balance is usually shifted towards female choice is the simple fact the if you don’t mate, you don’t get selected. Remember, selection is all about passing on your genetic material, and surviving is only important in that it gives you more time to reproduce. If you live forever, but never have any offspring, then you’re evolutionarily dead.

Why females are the choosy sexThe next important issue to address is why females are usually the ones who choose. The typical answer is, “Eggs are expensive, and sperm are cheap.” In other words, females invest more heavily in the offspring; therefore, they are the ones who choose the mate. To put this another way, females are physiologically limited in the number of offspring that they can produce, whereas males are only limited by the number of mates that they can obtain. If you think about humans for a second, females can have, at most, about one offspring a year (excluding twins, triplets, etc.). In contrast, males could, in theory, produce several hundred children a year because sperm is cheap and easy to produce. This means that females have a much greater investment in each offspring.

Think for a minute about an extremely polygamous, randomly mating bird (i.e., one where males and females both mate with many partners and females mate randomly). If a clutch of eggs is lost, the loss to the female is enormous because of the time, resources, etc. that went into producing those eggs. In contrast, the loss to the male is much less because all that he invested was sperm, and he has plenty more sperm to knock up other females with. By carefully selecting her mates, however, the female can maximize the chance that her offspring survive. Thus, it is in her best interest to make sure that her offspring get the best genes available. In contrast, it is in the male’s best interest to mate with as many females as possible.

Sex role reversal
Throughout this post, I have been acting as if it is always the female that chooses, but that’s not actually correct. There are several species of insect, bird, amphibian, mammal, and fish in which the male chooses (there are also probably some in other taxonomic groups). Based on what I just explained about female vs. male investment, it should not surprise you to learn that in these species, males do most or all of the parental care. In other words, they are the ones with the biggest investment in the offspring, which means that they are the ones who choose. Phalarope species (a variety of shorebird much like a plover) are a common example of this (Delehanty et al. 1998). In these species, the female is brighter than the males (though still fairly dull) and the female displays for the males. After mating and laying her eggs; however, she goes off to find another mate while the males take care of the eggs/young.

A comb-crested jacana (Irediparra gallinacea) near where I am currently living.

Jacanas are another good example (Haf et al. 2003). These super cool birds live on top of the lilies in tropical rivers and swamps, and the females (who are much larger than the males) control a territory with a harem of males. A female will mate with each of her males, but she doesn’t do any of the parental care. Rather, she leaves that to the males. Other than size, males and females look very much alike, so it is likely that they are selecting based on the territory that the females hold.

Summary
In short, sexual selection is simply a type of natural selection that acts on the traits responsible for obtaining a mate. Females are generally the sex that chooses because females have a greater investment in the offspring than the males. Also, females often choose exaggerated traits that are disadvantageous for the males because they use those traits to judge whether or not the male will produce high quality offspring. This results in a conflict where sexual selection is driving the evolution of elaborate features, while classical natural selection is driving the evolution of traits that maximize survivorship. Finally, although females are generally the choosy sex, there are exceptions, and in these exceptions, it is usually the males that do the selecting.

This post has only scratched the surface and I described most things using very broad brush strokes. So, if you found this interesting, I would encourage you to do some more reading (or at least watch Attenborough) because there are tons of great topics that I didn’t get a chance to talk about (sperm competition, dishonest signals, sneaker males, the effects of mating systems on sexual selection, sexual selection in humans, etc.).

8 Responses to Evolutionary mechanisms part 5: Sexual selection

That explains it! Why in the world do some women pick the men they do? Because they look at those men and think “Based on everything I’ve observed you should’ve been dead ages ago and I can’t even imagine how your parents both procreated and kept you alive. You must have quite the set of survival genes!”

Nice post. I will point out one thing: The reason females tend to choosy is that they have a lower variance in reproductive success. Females tend to be limited by fertility, males by mating success. Because males can mate with many females this means that at from a females perspective there are many males available more or less at all times. From a males perspective each receptive female is a scarce commodity. It may be that things like the high cost of eggs drives the difference in reproductive success, but ultimately it is this difference in the variance in reproductive success that is what is important.

I basically agree with you, but I think that you may have ultimate and proximate causes backwards. You said, “It may be that things like the high cost of eggs drives the difference in reproductive success, but ultimately it is this difference in the variance in reproductive success that is what is important.” I agree. The high cost of eggs is why females are limited by reproductive potential, while males are limited by the number of mates. However, that makes the cost of eggs the ultimate cause and the difference in reproductive success the proximate cause, because the cost of eggs causes the difference in reproductive potential.

I tried to make this clear when I said, “To put this another way, females are physiologically limited in the number of offspring that they can produce, whereas males are only limited by the number of mates that they can obtain.”

All in all a good post, but I must quibble with some of the semantics you use to dress your ideas. Let’s focus on this passage:

“In the sexy sons hypothesis, females are selecting a trait that they are attracted to because their sons will also get that attractive trait; whereas, in the good genes hypothesis, the females are simply using that trait as a way to assess whether or not a given male will produce high quality offspring.”

Why do so many biologists today speak in this manner? It seems highly conflated, from a physical perspective. In neither case are females attracted to a trait *because* of whatever selective trajectories shaped the typical psychological reactions of her species. Rather, a female of some species or another is attracted to some males moreso than others simply because, given her psychology, she finds certain ‘traits’ sexier than others. It would take a detailed course of investigation into the psychology of that species to get any more specific than this.

Biological selection certainly comes into play when we’re asking about what caused a particular species to fixate on the particularities of its psychological attractions. But this shorthand that is so often used to describe the process, in which selective causes are attributed to discrete behavioral actions, reads like a category error.

It strikes me as rather unlikely (and I expect that you will agree) that the individual female peacock is actually assessing the potential genetic worth of her fan-tailed suitor, and it is certainly not necessary that she should be doing so in order for natural selection to have shaped her species’ psychology such that she finds that tail alluring. Yet a literal reading of the text quoted above might be taken to imply exactly that…

“A female of some species or another is attracted to some males moreso than others simply because, given her psychology, she finds certain ‘traits’ sexier than others.” Sure, but why does she find those traits sexier? She does in fact find them attractive “because of whatever selective trajectories shaped the typical psychological reactions of her species.”

To be clear, females are not consciously thinking about genes, but that doesn’t mean that good genes aren’t the ultimate reason for her selective choices. Let’s say, for example, that in a population you have mostly dull males, but a few are bright. Further, assume that brightness is an honest signal (i.e., those males really do have the best genes). The females that happen to mate with those males will be selected for, because their children will get the good genes of the bright males. This will create a selection pressure for females to want bright males, which will in tern drive the selection of bright males. Thus, although females are not consciously thinking about genes, the ultimate reason that they like brightly colored males is because that is an indicator of the quality of males’ genes (assuming that the good genes hypothesis is correct). Thus, the females are using these traits to judge the quality of the males.

I am sorry to admit that I am not particularly swayed by the example you have offered just above. It seems to me every bit as circular as the logic of the sexy sons hypothesis (SSH) that you have previously critiqued. You have merely started with a foregone conclusion and derived from it a highly contrived example under which it is obviously true.

It seems to me much more reasonable to presume bright coloration that develops and becomes amplified over time as a sexual selection pressure favoring honest signaling builds momentum than to assume anything like the example you offer here. Selection pressures will rarely turn on or off like switches, and complex traits like a bright, advertisement plumage will rarely form wholesale in a single mutational leap of phenotypic faith.

To clarify my previous point, I agree there is a perspective under which the female of a species that has already settled into a dynamic consisting of advertisement displays “does in fact find them attractive ‘because of whatever selective trajectories shaped the typical psychological reactions of her species’” is for the most part valid. But as you allude to while writing of “the ultimate reason”, this perspective is that of ultimate causes.

Whereas a statement along the lines of “females are using these traits to judge the quality of males” is not structured as a statement of ultimate cause. It is structured as a statement of proximate cause – this is what the females are *doing*, and it is inaccurate to claim that what they are doing is “using these traits to judge the quality of males.” Past trajectories of selection have shaped their psychology such that they don’t have to.

I don’t have any problem with the first half of your conclusion: “[A]lthough females are not consciously thinking about genes, the ultimate reason that they like brightly colored males is because that is an indicator of the quality…” (Well, I do have a couple quibbles, but they are much subtler than the present topic, and probably too complex for the present format of discussion.) Indeed, I would say this statement reflects a relatively consistent manner of stating your case.

But the sentence that follows it does not follow from it. Rather, it conflates population-level dynamics and individual-level dynamics, and insodoing constitutes a category error.

I’m a bit confused. In regards to my example, you said, “bright coloration that develops and becomes amplified over time as a sexual selection pressure favoring honest signaling builds momentum than to assume anything like the example you offer here. Selection pressures will rarely turn on or off like switches, and complex traits like a bright, advertisement plumage will rarely form wholesale in a single mutational leap of phenotypic faith.” Isn’t that exactly what I described? A mutation arises which makes males that have it a bit brighter than their counterparts, and females who mate with those males have more offspring; therefore brightness gets selected for, and over time males become extravagant.

Later, you said, “it is inaccurate to claim that what they are doing is ‘using these traits to judge the quality of males.’ Past trajectories of selection have shaped their psychology such that they don’t have to.” I’m not sure what you mean here. What drove the past trajectories? Your answer seems to be void of an actual explanation for why females choose the traits that they do. You keep saying that they choose based on the psychology that resulted from their evolutionary trajectories, and I agree, but what caused those evolutionary trajectories?